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Biological Journal of the Linnean Society, 2020, XX, 1–10. With 2 figures. Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020

Trade-offs between burrowing and biting force in fossorial scincid ?

MARGOT LE GUILLOUX1, AURÉLIEN MIRALLES2, JOHN MEASEY3, BIEKE VANHOOYDONCK4, JAMES C. O’REILLY5, AURÉLIEN LOWIE6, and ANTHONY HERREL1,4,6,*,

1UMR 7179 C.N.R.S/M.N.H.N., Département Adaptations du Vivant, Bâtiment d’Anatomie Comparée, 55 rue Buffon, 75005, Paris, France 2Institut de Systématique, Evolution, Biodiversité, (UMR 7205 Muséum national d’Histoire naturelle, CNRS UPMC EPHE, Sorbonne Universités), CP30, 25 rue Cuvier 75005, Paris, France 3Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Private Bag X1, 7602 Matieland, Stellenbosch, South Africa 4Deparment of Biology, University of Antwerp, Universiteitsplein 1, B2610 Antwerpen, Belgium 5Department of Biomedical Sciences, Ohio University, Cleveland Campus, SPS-334C, Cleveland, 45701 Ohio, USA 6Department of Biology, Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium

Received 27 December 2019; revised 17 February 2020; accepted for publication 19 February 2020

Trade-offs are thought to be important in constraining evolutionary divergence as they may limit phenotypic diversification. The cranial system plays a vital role in many functions including defensive, territorial, predatory and feeding behaviours in addition to housing the brain and sensory systems. Consequently, the morphology of the cranial system is affected by a combination of selective pressures that may induce functional trade-offs. Limbless, head-first burrowers are thought to be constrained in their cranial morphology as narrow heads may provide a functional advantage for burrowing. However, having a wide and large head is likely beneficial in terms of bite performance. We used 15 to test for the existence of trade-offs between maximal push and bite forces, and explored the patterns of covariation between external head and body morphology and performance. Our data show that there is no evidence of a trade-off between bite and burrowing in terms of maximal force. Species that generate high push forces also generate high bite forces. Our data also show that overall head size covaries with both performance traits. However, future studies exploring trade-offs between force and speed or the energetic cost of burrowing may reveal other trade-offs.

ADDITIONAL KEYWORDS: covariation – cranial system – divergence – head-first burrowers – morphology – skink.

INTRODUCTION anatomical structures (Arnold, 1992; Van Damme et al., 2002, 2003). Previous studies have further suggested The phenotype of an organism reflects the selective that trade-offs may in some cases limit phenotypic pressures exerted by activities that are essential variation by constraining evolutionary divergence to its survival and its reproduction (Arnold, 1993). (Vanhooydonck et al., 2001; Levinton & Allen, 2005; Sometimes, however, the functional demands exerted Konuma & Chiba, 2007; Herrel et al., 2009). The by different performance traits may result in trade- cranial system plays a vital role in many activities offs. Indeed, functional trade-offs arise when different including defensive, territorial, predatory and feeding functions exert conflicting pressures on the same behaviours in addition to housing and protecting the brain and major sensory organs (Andrews et al., 1987; *Corresponding author. E-mail: [email protected] Cooper & Vitt, 1993; Herrel et al., 2007; Kohlsdorf

© 2020 The Linnean Society of London, Biological Journal of the Linnean Society, 2020, XX, 1–10 1 2 Burrowing and Biting in Scincid Lizards Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020 et al., 2008; Dumont et al., 2016). Consequently, the burrowing force. Consequently, trade-offs between these morphology of the cranial system is affected by these two performance traits, if present, are not mediated by combined selective pressures which may potentially direct functional conflict for the optimization of single induce functional trade-offs. functional trait. Rather, burrowers can be expected to The hypothetical trade-off between biting and have narrow heads for efficient soil penetration which borrowing performance is particularly interesting may come at a cost of bite force. in limbless burrowing . These organisms are Here, we test for the presence of a trade-off between obligate head-first burrowers and the evolution of maximal bite force and the maximal push force in a their morphology is thought to be constrained. Indeed, range of burrowing and leaf-litter dwelling . because the energy required for burrowing increases Scincid lizards represent an ideal study system as this exponentially with body and head diameter (Navas family includes a variety of ecologies and morphologies et al., 2004), having a thin body and a narrow head with quadrupedal surface-dwelling species, epigeal may provide a functional advantage for burrowing. Yet, serpentiform species with partially reduced front- and/ this is likely detrimental in terms of bite performance or hindlimbs, burrowing completely limbless species, and (Verwaijen et al., 2002; Navas et al., 2004; Herrel & a plethora of intermediate forms (Pianka & Vitt, 2003; O’Reilly, 2006; Vanhooydonck et al., 2011; Baeckens Miralles et al., 2015; Wagner et al., 2018; Bergmann & et al., 2017; Hohl et al., 2017). Maximum bite force has Morinaga, 2019). At least 15 independent evolutions of a been suggested to limit the type and size of food an serpentiform body form have taken place within the group can eat (Herrel et al., 1999, 2001, 2008; Aguirre (Benesh & Withers, 2002; Miralles et al., 2012) allowing et al., 2003; McBrayer & Corbin, 2007; Edwards et al., for a robust framework to test for associations between 2013). Consequently, a cranial form optimized for soil life-style, performance and morphology. Consequently, penetration may compromise the types of food an we also explore the patterns of covariation between head animal can eat and vice versa (Andrews et al., 1987; and body morphology and the two performance traits Barros et al., 2011; Baeckens et al., 2017). studied here (bite force and push force). Burrowing is a complex behaviour that remains rather poorly understood in limbless head-first burrowing vertebrates (but see for example Gaymer (1971); Gans (1973); O’Reilly et al. (1997); Teodecki et al. MATERIALS AND METHODS (1998); Navas et al. (2004); De Schepper et al. (2005)). Animals The maximal push force that an animal can generate is likely important as it may allow an animal to penetrate Morphological measurements were performed on 180 a greater variety of soil types, and thus expand its individuals and performance measurements were resource base in terms of potential habitat and food obtained for 171 individuals for bite forces and 159 for resources. As limbless species burrow by recruiting push forces across 14 different species (Table 1). Animals muscles along the long axis of the body (Rieppel, 1981; were sampled between 2000 and 2017. The specimens Navas et al., 2004; Vanhooydonck et al., 2011; Hohl were adults of often unknown sex. Data were collected in et al., 2017), the diameter and size of the body should situ in the field or in the lab for species that were obtained be related to the maximal push force it can generate. through the pet trade. An additional five individuals of However, to facilitate soil penetration the width of the the species Pygomeles braconnieri from the collections of head should rather be narrow as this optimizes the the National Museum of Natural History in Paris were pressure for a given force (e.g. Measey & Herrel, 2006; used for morphological measurements. Herrel & Measey, 2010; Barros et al., 2011). Moreover, the speed by which it can penetrate the soil (and not only Morphometrics the force generated) is also likely a factor significantly contributing to the burrowing performance (Ducey Each individual was weighed using an electronic et al., 1993; Teodecki et al., 1998; Vanhooydonck et al., balance (Ohaus, ± 0.1 g). Head length, head width, 2011). Although few quantitative data exist, a previous head depth and lower jaw length were measured using study suggested the presence of a trade-off between bite a digital caliper (Mitutoyo, ± 0.01 mm) as described force and burrowing speed in a limbless skink, Acontias previously (Herrel and Holanova, 2008). The snout- percevali, mediated by the conflicting demands on vent length was measured by stretching the animals head dimensions (Vanhooydonck et al., 2011). However, along a ruler (± 1 mm). whether this is more generally the case and whether trade-offs also exist between bite force and push force remains unknown. As burrowing force is dependent Maximal push force on the axial musculature, different anatomical traits Maximal push forces were measured in the field or in the are responsible for the generation of bite force vs. lab following the protocol described in Vanhooydonck

© 2020 The Linnean Society of London, Biological Journal of the Linnean Society, 2020, XX, 1–10 M. LE GUILLOUX ET AL. 3 Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020 Bite force (N) 9.36 ( N = 1) 1.27 ( N = 1) 18.39 ± 3.59 ( N = 5) 1.16 ± 0.40 ( N = 5) 3.01 ± 1.60 ( N = 32) 0.73 ± 0.19 ( N = 42) 0.45 ± 0.12 ( N = 9) 8.99 ± 1.77 ( N = 6) 0.93 ± 0.25 ( N = 6) 10.08 ± 3.06 ( N = 12) 6.82 ± 4.19 ( N = 13) 4.12 ± 0.75 ( N = 17) 12.33 ± 6.45 ( N = 10) 1.33 ± 0.70 (N = 11) (N) Push force 7.72 ± 2.04 ( N = 5) 0.56 ± 0.20 ( N = 5) 2.11 ± 1.02 ( N = 32) 0.51 ± 0.25 ( N = 41) 0.32 ± 0.08 ( N = 8) 3.13 ± 0.47 ( N = 3) 1.58 ± 0.33 ( N = 5) 5.32 ± 0.85 ( N = 12) 4.56 ± 1.39 ( N = 14) 2.46 ± 0.75 ( N = 17) 1.56 ± 1.25 ( N = 7) 7.50 ( N = 1) 0.55 ( N = 1) 0.36 ± 0.16 ( N = 8) (mm) 3.55 ( N = 1) Body diameter 14.76 ± 1.35 ( N = 5) 4.28 ± 0.37 ( N = 5) 4.27 ± 0.72 ( N = 32) 3.38 ± 0.48 ( N = 47) 2.91 ± 0.17 ( N = 9) 7.26 ± 1.30 ( N = 6) 3.56 ± 0.39 ( N = 6) 9.28 ± 0.99 ( N = 12) 10.77 ± 3.26 ( N = 16) 7.45 ± 0.65 ( N = 17) 6.97 ± 1.32 ( N = 7) 7.99 ± 3.85 ( N = 6) 3.84 ± 0.66 ( N = 12) (g) Mass 1.00 ( N = 1) 18.75 ± 3.96 ( N = 5) 1.95 ± 0.64 ( N = 5) 3.42 ± 1.48 ( N = 32) 1.39 ± 0.45 ( N = 47) 0.92 ± 0.19 ( N = 9) 9.74 ± 2.85 ( N = 6) 2.68 ± 1.09 ( N = 6) 16.87 ± 5.07 ( N = 12) 10.28 ± 6.88 ( N = 16) 4.66 ± 1.02 ( N = 17) 9.83 ± 6.55 ( N = 10) 12.78 ± 7.34 ( N = 6) 1.56 ± 0.73 ( N = 11) Lower jaw Lower jaw 6.40 ( N = 1) length (mm) 18.44 ± 1.47 ( N = 5) 5.70 ± 0.34 ( N = 5) 4.67 ± 0.77 ( N = 32) 5.09 ± 0.76 ( N = 47) 3.99 ± 0.50 ( N = 9) 7.67 ± 1.16 ( N = 6) 5.40 ± 0.86 ( N = 6) 13.25 ± 0.76 ( N = 7) 12.96 ± 3.04 ( N = 16) 9.97 ± 0.71 ( N = 17) 12.64 ± 2.29 ( N = 10) 9.40 ± 1.98 ( N = 6) 5.46 ± 0.58 ( N = 12) Head depth (mm) 9.92 ± 0.88 ( N = 5) 3.23 ± 0.86 ( N = 5) 1.98 ± 0.27 ( N = 32) 2.54 ± 0.26 ( N = 47) 2.13 ± 0.07 ( N = 9) 4.56 ± 0.55 ( N = 6) 2.67 ± 0.33 ( N = 6) 6.98 ± 0.70 ( N = 12) 6.53 ± 1.95 ( N = 16) 5.05 ± 0.24 ( N = 17) 6.20 ± 1.19 ( N = 10) 5.06 ± 0.99 ( N = 6) 2.83 ( N = 1) 2.62 ± 0.42 ( N = 12) Head width (mm) 10.65 ± 0.75 ( N = 5) 3.60 ± 0.20 ( N = 5) 3.39 ± 0.54 ( N = 32) 3.01 ± 0.29 ( N = 47) 2.60 ± 0.09 ( N = 9) 5.81 ± 0.90 ( N = 6) 3.18 ± 0.37 ( N = 6) 8.00 ± 0.75 ( N = 12) 7.76 ± 2.18 ( N = 16) 5.93 ± 0.33 ( N = 17) 7.68 ± 1.55 ( N = 10) 6.25 ± 1.44 ( N = 6) 3.32 ( N = 1) 3.22 ± 0.58 ( N = 12) (mm) 6.81 ( N = 1) Head length 7.27 ± 0.49 ( N = 5) 6.70 ± 0.80 ( N = 32) 5.95 ± 0.91 ( N = 47) 5.52 ± 0.29 ( N = 9) 10.43 ± 1.08 ( N = 6) 6.76 ± 0.99 ( N = 6) 13.88 ± 1.34 ( N = 12) 11.85 ± 2.76 ( N = 16) 9.90 ± 0.48 ( N = 17) 12.40 ± 2.40 ( N = 10) 10.61 ± 1.72 ( N = 6) 6.18 ± 0.57 ( N = 12) 18.76 ± 0.72 ( N = 5) SVL (mm) 61.58 ( N = 1) 116.12 ± 12.10 ( N = 5) 171.30 ± 34.42 ( N = 32) 108.34 ± 16.64 ( N = 47) 106.33 ± 10.49 ( N = 9) 194.24 ± 16.34 ( N = 6) 195.33 ± 48.57 ( N = 6) 246.83 ± 12.48 ( N = 12) 80.88 ± 24.41 ( N = 16) 83.41 ± 5.73 ( N = 17) 83.64 ± 18.88 ( N = 10) 109.67 ± 37.11 ( N = 6) 74.56 ± 10.67 ( N = 12) 92.20 ± 3.04 ( N = 5) Mean and standard deviation of morphological and functional data for the 14 species included in this study Mean and standard deviation of morphological functional data for the 14 species included

caecus lomiae vermis sepsoides sundevallii braconnieri montispectus Table 1. Table Species Acontias kgalagadi Typhlosaurus Typhlosaurus Acontias litoralis Typhlosaurus Typhlosaurus Acontias meleagris Typhlosaurus Typhlosaurus Acontias percivali Chalcides ocellatus Chalcides Mochlus Mochlus Pygomeles bipes Scelotes scincus

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Figure 1. Phylogeny used in the analyses modified from Pyron et al. (2013). et al. (2011). Measurements of peak push forces during Maximal bite force burrowing were made using a custom piezoelectric Maximal bite forces were measured in the field or force platform (Kistler Squirrel force plate, ± 0.1 N, the lab following Herrel et al. (1999). In brief, in vivo Kistler Inc., Switzerland). The force platform was bite forces were measured using an isometric Kistler positioned on a custom-designed metal base and force transducer (type 9203, Kistler Inc.) mounted connected to a charge amplifier (Kistler Charge on a purpose-built holder and connected to a Kistler Amplifier type 9865, Kistler Inc.). A Perspex block with charge amplifier (type 5058 A, Kistler Inc.). Biting 1 cm-deep holes of different diameters was mounted on causes the upper plate to pivot around the fulcrum, the force plate, level with the front edge. One of the and thus pull is exerted on the transducer. Capture holes was loosely filled with soil from the container of of the animals typically resulted in a characteristic the animal that was tested. A Perspex tunnel with a threat response where the jaws are opened maximally. diameter similar to the maximal body diameter of the The free end of the holder was then placed between test animal was mounted on the metal base in front the jaws of the animal, which immediately resulted of (but not touching) the force plate, and aligned with in fierce and prolonged biting. The gape angle (± the soil-filled hole in the Perspex block. First, a skink 30 °) and the place of application of the bite force was was introduced into the tunnel and allowed to move standardized with animals always biting at the tips through it until reaching the soil-filled chamber. Next, of the jaws. Measurements were repeated five times the animal was stimulated to burrow into the soil by for each animal and the maximum value recorded was tapping the end of the tail sticking out of the tunnel, considered to be the maximal bite force for that animal. or by prodding the animal inside the tunnel with the blunt end of a thin wooden stick. Forces were recorded during a 60 s recording session at 500 Hz, and three Analyses trials were performed for each individual, with at Morphometric and force data were Log10- least 1 h between trials. Forces were recorded in three transformed before analysis to ensure normality and dimensions using the Bioware software (Kistler Inc.). homoscedasticity. For each individual we then extracted the highest All analyses were performed in R (v.3.4.0) while peak resultant force across all trials as an indicator of taking into account the phylogenetic relationships that animal’s maximal push force. among species. The phylogenetic framework

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Figure 2. Phylogenetic regressions of species averages of maximal bite force against maximal push force. (A) Absolute push force is significantly correlated with absolute bite force. (B) Residual bite force is significantly and positively correlated with residual push force when correcting for overall snout-vent length. (C) Residual bite force is no longer related to variation in residual push force when corrected for variation in body mass.

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Figure 3. Covariance between morphological and performance data. (A) Phylogenetic two-block partial least square analysis between morphology and performance illustrating that more robust species (i.e. with greater body mass and bigger heads) produce greater push and bite forces. (B) Two-block partial least square analysis on the force and morphological data corrected for variation in snout-vent length. Species with relatively higher mass, heads size and body diameter produce greater bite and push forces. (C) Two-block partial least square analysis on the force and morphological data corrected for variation in body mass showing that species that are relatively more elongate (higher snout-vent length for their mass) show relatively higher push forces. In contrast, species that are stockier, less elongate and with bigger heads produce relatively higher bite forces. used was obtained from the molecular data set include only species for which we had performance of Pyron et al. (2013); Fig. 1. This required the and morphological data. First, a phylogenetic reconstruction of a phylogeny by pruning the tree to generalized least squares (PGLS) regression was

© 2020 The Linnean Society of London, Biological Journal of the Linnean Society, 2020, XX, 1–10 M. LE GUILLOUX ET AL. 7 Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020 run in R (function gls with corBrownian in Phytools appear to have relatively large bite forces but low (Revell, 2012)) with the mean maximal push force push forces. per species against mean maximal bite forces to test for the presence of a trade-off between bite and push force. To test for co-variation between Covariation between morphology and morphology and performance we ran a phylogenetic performance two-block partial least squares analysis (φ2bPLS) The phylogenetic 2BPLS analysis was significant using the function ‘phylo.integration’ implemented (rPLS = 0.983, P = 0.001). Heavier, larger and wider in ‘geomorph’ in R (Adams et al., 2013). This method animals with longer, taller and wider heads produce quantifies the degree of association between two data larger forces (Fig. 3A). The 2BPLS analysis run on matrices. It is a descriptive multivariate analysis the size-corrected data was also significant (rPLS = robust to multicollinearity between variables and 0.969, P < 0.001; Fig. 3B). This analysis indicates that therefore suitable for the use of morphometric and the maximal push force and the maximal bite force performance variables. The analysis generates axes co-vary, both principally with overall head and body that explain the covariance between the two data robustness, with animals that are more elongate matrices. producing relatively lower push and bite forces. An As body size simultaneously impacts head and analysis on the size corrected data using body mass body dimensions and forces, we ran PGLS analyses was also significant (rPLS = 0.73, P = 0.012), yet with snout-vent length (SVL) or body mass as our showed a different pattern. This analysis shows that predictor and morphometric and performance traits more elongate animals produce relatively higher as our independent variables and extracted the push forces whereas the more robust limbed species unstandardized residuals. Next, we used a Pearson with wide heads and bodies produce low push but correlation test to explore the existence of a trade- high bite forces for their body mass (Fig. 3C). off between our two residual performance traits independent of variation in overall body size. Finally, we ran a two-block partial least squares analyses (2BPLS) on the residual data to explore patterns of DISCUSSION covariation between morphology and performance Our results, based on a broad range of burrowing and independent of variation in overall size using ‘two.b.pls’ leaf-litter dwelling skinks, show that there is no direct script of the ‘geomorph’ package (Adams et al., 2013), trade-off between bite force and burrowing force in and ‘pls2B’ script of the ‘Morpho’ package (Schlager, this group. Species that produce strong push forces 2013) in R. are also those which produce strong bite forces in both absolute and relative terms. These results suggest that whereas bite force may trade-off with burrowing RESULTS speed (Teodecki et al., 1998; Vanhooydonck et al., 2011) this may not be the case for push force. Indeed, the Trade-offs between bite force and push force same traits that favour increased bite force (large, The linear regression taking into account phylogeny robust heads and wide bodies) also appear to favour shows that maximum push force is positively high push forces, at least in absolute terms. This correlated with maximal bite force (PGLS: r = 1.36, makes intuitive sense as the muscles used to generate P < 0.001), suggesting that species that produce both bite and push force are positioned to the lateral strong push forces are also those who produce strong side of the body in scincid lizards (Huyghe et al., 2009; bite forces (Fig. 2A). Analyses performed on the snout- Vanhooydonck et al., 2011). For example, the external vent length corrected data show a similar result adductor muscle is one of the largest contributors to (r = 0.89, P < 0.001) with animals that bite harder overall bite force generation and lies external to the for a given size also being better pushers (Fig. 2B). mandible (Vanhooydonck et al., 2011). Similarly, the However, when correcting force measurements for iliocostalis and longissimus muscles that generate body mass, residual bite force was no longer correlated the push forces measured are also positioned laterally with residual push force (r = -0.63, P = 0.053; Fig. to the vertebral column. Consequently, wider heads 2C). An inspection of the plot (Fig. 2C) suggests that and wider bodies should induce an increase in both more elongate and smaller species like Typhlosaurus absolute bite and push force. However, whereas these vermis and T. lomiae as well as Acontias litoralis traits may indeed favour absolute force, the speed and A. kgalagadi tend to have relatively higher by which animals can penetrate the soil may be push forces whereas the stockier, larger species like negatively impacted by the presence of wider heads Scincus scincus, A. meleagris, and Mochlus sundevalli and bodies (Teodecki et al., 1998; Vanhooydonck et al.,

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ACKNOWLEDGMENTS Traits affecting bite and burrow performance Despite the absence of trade-offs, we hypothesized that We would like to thank Günter Wagner and an morphological traits that co-vary with each type of anonymous reviewer for helpful and constructive performance trait might be different. In contrast to our comments on a previous version of this manuscript prediction, the phylogenetic 2BPLS analysis showed and Anne-Claire Fabre for extensive help with the that all traits covaried with both forces, especially analyses and without whom this paper would not have body mass. Heavier, larger and wider animals with been possible. South African fieldwork was conducted long, tall and wide heads produced greater forces in in under provincial research permits in the Western absolute terms. However, analyses performed on the Cape (AAA007-00035-0035), Limpopo (333-00015) size corrected data showed different results. Indeed, and Northern Cape (FAUNA 1243/2008). AH and whereas the relative mass and the diameter of the JM thank Krystal Tolley and the National Research body and head relative to the length of the animal Foundation (NRF) of South Africa (South African appear to drive both variation in bite force and push Biosystematics Initiative-SABI, Key International force, as with absolute data, when correcting for body Science Collaboration-KISC), and ethics clearance mass this was no longer the case. More robust and from SANBI (0010/08). less elongate limbed species with wide and deep heads FUNDING This work was supported by a grant like Chalcides ocellatus, Scincus scincus or Mochlus from Agence Nationale de la Recherche under sundevalli produce relatively high bite, yet low push the LabEx ANR-10-LABX-0003-BCDiv, in the forces (see Fig. 3C). This is expected as it had been program ‘Investissements d’avenir’ n\u0001 shown that the maximal bite force generated by an ANR-11-IDEX-0004-02. individual is determined by its head dimensions (Verwaijen et al., 2002; Navas et al., 2004; Herrel & O’Reilly, 2006; Vanhooydonck et al., 2011; Baeckens REFERENCES et al., 2017; Hohl et al., 2017). Maximum push force Adams DC, Otarola-Castillo E, Paradis E. 2013. Geomorph: has, however, been suggested to be determined by the an R package for the collection and analysis of geometric total length of the body (Rieppel, 1981; Navas et al., morphometric shape data. Methods in Ecology and Evolution 2004; Measey & Herrel, 2006; Barros et al., 2011; 4: 393–399.

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